Bottom Line:
There is no consistent tendency of evolution towards increased genomic complexity, and when complexity increases, this appears to be a non-adaptive consequence of evolution under weak purifying selection rather than an adaptation.Several universals of genome evolution were discovered including the invariant distributions of evolutionary rates among orthologous genes from diverse genomes and of paralogous gene family sizes, and the negative correlation between gene expression level and sequence evolution rate.Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future.

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA. koonin@ncbi.nlm.nih.gov

ABSTRACTComparative genomics and systems biology offer unprecedented opportunities for testing central tenets of evolutionary biology formulated by Darwin in the Origin of Species in 1859 and expanded in the Modern Synthesis 100 years later. Evolutionary-genomic studies show that natural selection is only one of the forces that shape genome evolution and is not quantitatively dominant, whereas non-adaptive processes are much more prominent than previously suspected. Major contributions of horizontal gene transfer and diverse selfish genetic elements to genome evolution undermine the Tree of Life concept. An adequate depiction of evolution requires the more complex concept of a network or 'forest' of life. There is no consistent tendency of evolution towards increased genomic complexity, and when complexity increases, this appears to be a non-adaptive consequence of evolution under weak purifying selection rather than an adaptation. Several universals of genome evolution were discovered including the invariant distributions of evolutionary rates among orthologous genes from diverse genomes and of paralogous gene family sizes, and the negative correlation between gene expression level and sequence evolution rate. Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future.

Mentions:
Joint analysis of the novel class of phenomic variables characterized by systems biology and the measures of gene evolution such as sequence evolution rate and propensity for gene loss revealed a rather unexpected structure of correlations [(81,254,255); Figure 3A]. Despite the intuitive link between the rate of evolution and gene dispensability [‘important’ genes would be expected to evolve slower than less important ones (256)], only a weak link (at best) between these characteristics was detected (257–259). The link between evolution rate and functional importance of a gene deserves further investigation because comprehensive analysis reveals a measurable phenotypic effect of knockout of virtually each yeast gene under some conditions (260). However, regardless of the outcome of such studies, clearly, this link is subtle, even if it turns out to be robust. In contrast, the strongest correlation in all comparisons between evolutionary and phenomic variables was seen between gene expression level and sequence evolution rate or propensity for gene loss: highly expressed genes, indeed, tend to evolve substantially slower than lowly expressed genes (254,261). This finding is buttressed by the observations of a positive correlation between sequence divergence and the divergence of expression profiles among human and mouse orthologous genes (252) and the comparatively low rates of expression profile divergence in highly expressed genes (262).Figure 3.

Mentions:
Joint analysis of the novel class of phenomic variables characterized by systems biology and the measures of gene evolution such as sequence evolution rate and propensity for gene loss revealed a rather unexpected structure of correlations [(81,254,255); Figure 3A]. Despite the intuitive link between the rate of evolution and gene dispensability [‘important’ genes would be expected to evolve slower than less important ones (256)], only a weak link (at best) between these characteristics was detected (257–259). The link between evolution rate and functional importance of a gene deserves further investigation because comprehensive analysis reveals a measurable phenotypic effect of knockout of virtually each yeast gene under some conditions (260). However, regardless of the outcome of such studies, clearly, this link is subtle, even if it turns out to be robust. In contrast, the strongest correlation in all comparisons between evolutionary and phenomic variables was seen between gene expression level and sequence evolution rate or propensity for gene loss: highly expressed genes, indeed, tend to evolve substantially slower than lowly expressed genes (254,261). This finding is buttressed by the observations of a positive correlation between sequence divergence and the divergence of expression profiles among human and mouse orthologous genes (252) and the comparatively low rates of expression profile divergence in highly expressed genes (262).Figure 3.

Bottom Line:
There is no consistent tendency of evolution towards increased genomic complexity, and when complexity increases, this appears to be a non-adaptive consequence of evolution under weak purifying selection rather than an adaptation.Several universals of genome evolution were discovered including the invariant distributions of evolutionary rates among orthologous genes from diverse genomes and of paralogous gene family sizes, and the negative correlation between gene expression level and sequence evolution rate.Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future.

Affiliation:
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USA. koonin@ncbi.nlm.nih.gov

ABSTRACTComparative genomics and systems biology offer unprecedented opportunities for testing central tenets of evolutionary biology formulated by Darwin in the Origin of Species in 1859 and expanded in the Modern Synthesis 100 years later. Evolutionary-genomic studies show that natural selection is only one of the forces that shape genome evolution and is not quantitatively dominant, whereas non-adaptive processes are much more prominent than previously suspected. Major contributions of horizontal gene transfer and diverse selfish genetic elements to genome evolution undermine the Tree of Life concept. An adequate depiction of evolution requires the more complex concept of a network or 'forest' of life. There is no consistent tendency of evolution towards increased genomic complexity, and when complexity increases, this appears to be a non-adaptive consequence of evolution under weak purifying selection rather than an adaptation. Several universals of genome evolution were discovered including the invariant distributions of evolutionary rates among orthologous genes from diverse genomes and of paralogous gene family sizes, and the negative correlation between gene expression level and sequence evolution rate. Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future.